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https://doi.org/10.1007/s11104-023-05988-7
METHODS PAPER
Received: 8 January 2023 / Accepted: 10 March 2023 / Published online: 5 April 2023
© UT-Battelle, LLC 2023
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avenue necessary to fill the asymmetrical knowledge and ecology fields, the specific correlations among
gaps in belowground performance of plant systems. and larger impacts of variation in these properties
is poorly understood. Having the ability to easily
Keywords Laser-induced breakdown spectroscopy · and quickly characterize the variation in composi-
Rapid phenotyping · Bioenergy crops · Plant nutrients tion of and correlation among the nutrient elements
in various plant tissue types and soil sample types is,
therefore, expected to greatly aid in discerning the
Introduction critical components within coupled biogeochemi-
cal, structure-function, plant-soil processes with the
Plant performance, including growth and stress most potential to improve 1) sustainable production
response, ability is determined by levels and distri- of bioenergy and food crops, 2) soil health and phy-
bution of various nutrients elements; macronutrients toremediation, and 3) carbon sequestration potential
[nitrogen (N), phosphorus (P), potassium (K), cal- in soils. In the context of the latter, C storage capac-
cium (Ca), sulfur (S), magnesium (Mg), carbon (C), ity of soils is known to be influenced by range of soil
oxygen (O), hydrogen (H)] and micronutrients [such properties including nutrient reserves (Lal 2018).
as silicon (Si), iron (Fe), boron (B), chlorine (Cl), For example, C sequestration ability was reported to
manganese (Mn), zinc (Zn), copper (Cu), molybde- be limited both directly by N and indirectly by nutri-
num (Mo), nickel (Ni)]. These elements are essential ents such as P, Mo, and K needed to in turn support
to plant growth and survival and range in their func- N fixation (van Groenigen et al. 2006). Ability to
tions from structural to that of metabolic/enzymatic. characterize elemental distribution in various plant
Nutrition status of plants and elemental composition tissues and co-assess with spatiotemporal variation in
of their tissues is a factor of plant genetics, environ- soil and rhizosphere properties is immensely useful in
mental variations, and the dynamic interactions of the plant and ecosystem science communities’ quest
the two in the rhizosphere (Lynch 2019). Plant genet- to correlate above and belowground processes. Such
ics contribute to both the active and passive nutrient analytical capabilities are also integral to measuring
transport mechanisms throughout radial and vertical and validating the effectiveness of crop biotechnology
plant axes by determining influx and efflux transport- (e.g., plant chemistry)- and management (e.g., bio-
ers, ion and water uptake efficiency, mineral assimi- char amendments)- based strategies to enhance soil
lation, vasculature and suberization patterns (Morgan carbon sequestration (Jansson et al. 2010).
and Connolly 2013; Che et al. 2018; Harman-Ware Laser-induced breakdown spectroscopy (LIBS)
et al. 2021). The plasticity of genetically determined is an optical spectroscopy technique well suited for
plant traits is in turn known to be influenced by vari- rapid elemental composition measurements. LIBS
ation in the surrounding environment. These envi- is performed by focusing a nanosecond pulsed laser
ronmental factors include soil characteristics (chemi- onto a sample surface, at which point the energy
cal, physical and microbiome composition), climate density is enough to ablate the material and form a
(temperature, moisture, etc.), and the highly dynamic plasma plume. This short-lived plasma will quickly
abiotic and biotic interaction space of the rhizosphere cool and emit characteristic emissions which can be
(Kuppe et al. 2022). Microbiome composition, micro- measured with a spectrometer. The resultant spec-
bial colonization, and activity in root endosphere, tra provide an elemental fingerprint of the tested
rhizosphere, and soil have plant and ecosystem level sample. LIBS boasts robust traits such as requiring
consequences. Beneficial root colonizers are known little-to-no sample preparation, being sensitive to
to impact plant performance and nutrient status, and nearly every element in the periodic table, and being
vice versa plant nutrient uptake mechanisms and useful regardless of sample form (i.e., solids, liq-
suberization impact microbiome composition (Qu uids, and gases). The sensitivity of LIBS for detect-
et al. 2020; Salas-González et al. 2021). ing light elements is of great benefit to its applica-
While the interdependent relationships among tion on biological samples. LIBS is capable of both
structural, chemical, and functional properties of plant qualitative and quantitative analysis; for the latter
root, root rhizosphere, and soil have generally been matrix matched standards are needed for calibration
acknowledged in plant physiology, crop productivity, such that the ablation process for the calibration set
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Plant Soil (2024) 495:3–12 5
and analyzed samples are the same, or very simi- plant chemistry. To test the applicability of LIBS as
lar. When a proper calibration is performed LIBS a rapid in situ elemental profiling technique of small
has been shown to have detection limits on the volume samples for bioenergy research, we leveraged
10–100 ppm scale. here plant and soil samples from greenhouse grown
The use of LIBS in the detection of elements plants of a woody bioenergy crop species, Populus
in biological and environmental samples has been trichocarpa. The ultimate goal of this work would
demonstrated previously (Martin and Cheng 2000; be to expand the testing procedure described here to
Cremers and Radziemski 2013; Miziolek et al. the testing of hundreds of field samples to provide a
2006; Hahn 2009; Hahn and Omenetto 2012; new rapid phenotyping avenue necessary to fill the
Modlitbová et al. 2020, 2021). Specifically, LIBS asymmetrical knowledge gaps in belowground perfor-
has been used to detect soil carbon which has mance of plant systems.
been identified by soil scientist in the last decade
as the opportunity to manage terrestrial C stocks
as a strategy to mitigate increasing CO2 concen- Materials and methods
trations in the atmosphere (Paustian et al. 1997;
Conant et al. 2001; Lal 2004; West et al. 2008; This study used exemplar samples (i.e., Root 1 and
Martin et al. 2003, 2007, 2010, 2013). Further- Root 2) from developmentally variable sample types,
more, since plants absorb nutrients in substantial plants were either grown in water or potting mix.
amounts along with nonessential and essential ele- Hydroponic root tissue sample (Root 1) was obtained
ments in trace amounts, there have been a number from a young four-week old P. trichocarpa wild-
of studies published that demonstrate the ability of type plant growing in distilled water in the green-
LIBS to scan leaves and stems to show the distribu- house, and considered younger, tender root with
tion and accumulation of these elements in spruce minimal secondary growth and lignification. Root
(Krajcarova et al. 2013), in poplar leaves and bark 2 was obtained from a 16-week old plant growing
samples (Martin et al. 2017), and in switchgrass in soil pot, and considered older, mature root with
(Martin et al. 2021). A recent study showed that pronounced secondary growth and lignification as
the elemental concentrations obtained by LIBS in shown in Fig. 1. Sample Shoot 1 was obtained from
plant materials correlated well to other elemental the same 16-week old greenhouse plant. For gener-
techniques such as inductively coupled plasma- ating samples from the 16-week old plant grown in
mass spectrometry, atomic absorption spectroscopy soil potting mix, greenwood stem cuttings were veg-
and neutron activation analysis techniques that etatively propagated and grown in soil pots with pot-
are the gold standard analytical methods used for ting mix (Fafard Professional Potting Mix, Sun Gro
the quantification of these elements (Martin et al.
2021). Other recent works have shown LIBS to be
a useful tool for mapping the elemental distribution
in plant samples; while the results are very use-
ful these measurements necessitate careful sample
preparation (e.g., mounting, embedding in wax, or
freezing), precise sample stages for high resolution
mapping, and the measurements can take longer
than traditional LIBS measurements (Krajcarova
et al. 2013; Singh et al. 2019, 2021; Modlitbová
et al. 2020, 2021). While these studies provide
high resolution mapping at the expense of time and
throughput, we seek to benefit from LIBS’ vast ele-
mental sensitivity and rapid analysis time.
The goal of this research is to demonstrate the
Fig. 1 Photo of as collected samples mounted onto slide for
high-throughput capability of LIBS for biological LIBS analysis. The scale bar is provided for reference and is
samples with no sample preparation rapidly revealing equal to the diameter of the pellet tested
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Horticulture, Agawam, MA, USA) for four months altering the laser’s Q-switch delay and was set to
under controlled greenhouse temperature of ~25 °C 60 mJ. A greater shot energy was used due to mois-
and light cycles of 16 h day length as previously ture impacting the plasma formation. The translation
described (Payyavula et al. 2022). stage allowed for sample surfaces to be scanned along
Samples were taken from plants of different their length with single shots in 300 μm steps. The
maturities to investigate any differences in the laser soil pellet was scanned in a 6 × 6 pattern (300 μm
sampling to inform future experiments. The stem and spacing) with a 5 shot average spectrum saved at
root samples were freshly harvested from greenhouse each shot location. The included imaging kit allowed
grown plants using a scalpel and blade, and promptly for precise locations to be selectively tested and the
transferred to double distilled water. The soil sam- focal point of the laser to be properly aligned with
ple was scooped from the top one inch of potted the sample surface. During all tests air was passed at
soil plants using a spatula. Fresh samples were kept 10 L min−1 across the top of the shooting location to
at room temperature and transported within minutes prevent dust accumulation on optical components.
to LIBS laboratory for further processing. For this
study, only technical replicates were used (i.e., the
samples were tested multiple times) whereas in future Results
studies for biological insights five or more biological
replicates of each sample will be minimally required To better evaluate the ability to use LIBS for rapid
to derive statistically supported differences in nutrient in situ analysis of plant samples, the root and shoot
information, which is a future direction of this work. samples were measured first with minimal sample
This also emphasizes the need for a high throughput preparation and then with more specific preparation
method to not only test hundreds of different plant to compare.
samples but also their replicates.
First, the samples evaluated in this test study were Fresh samples
examined with as little sample preparation as possi-
ble. Excess liquid was removed from the as collected The raw samples were scanned along their length
samples’ surfaces and then they were mounted onto shown in Fig. 1. The averaged spectra, normalized
microscope slides using double-sided tape for initial the largest emission (393.38 nm Ca I), are shown
analysis. A photo of the as collected samples is shown in Fig. 2. Figure 2(a) shows the three spectra with a
in Fig. 1. The soil sample was pressed onto the tape, 0.2 baseline offset to better see the similarities in the
but residual moisture in the soil caused issues with emission profiles. The spectra are dominated by the
adhesion. Following the initial measurements, the emissions from Ca, Mg, C, Na, H, N, K, and O. These
samples were then cross sectioned and dried for addi- elements correspond to major macronutrient species.
tional tests. This second set of test samples was used The H, N, and O emissions are attributed to both
to determine if more sample preparation may enhance these species in the ablated sample and the atmos-
the LIBS results. For this second set of tests the dried phere where the plasma formed. Figure 2(b-e) pro-
soil was pressed into a pellet (13 mm in diameter). vide a closer look at specific spectral windows. Here,
All samples were testing using the LIBS-8 sys- the emissions of additional micronutrients Fe, Si, and
tem from Applied Photonics. This system included a Al can be seen.
1064 nm Nd:YAG laser (Litron Nano) with a 100 μm Minor differences in the average spectra can
spot size, an imaging kit from Applied Photonics, a be seen at this scale. Root 1 and Root 2 both show
motorized XYZ translation stage, and a multichan- the presence of Fe, Si and Al whereas Shoot 1 does
nel spectrometer. This multichannel spectrometer not show these micronutrients. The average spectra
includes eight Avantes miniature Czerny-turner spec- appear to only show Fe in Root 1, but upon further
trometers with CMOS detectors, ranging in wave- investigation it was found that the Fe in Root 1 was
length from 190 to 1000 nm with a resolution ranging not homogenously dispersed rather it was concen-
from 0.05–0.17 nm. For these tests the spectrometer trated in approximately 4 mm of the scanned length
gate delay was set to 3 μs and the exposure time was (Fig. 3). Fe is similarly located in a concentrated loca-
set to 25 μs. The laser energy was controlled through tion in Root 2, but the size and concentration of this
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Fig. 2 Normalized and averaged LIBS spectra of the freshly prepared samples; a stacked plot to show similarity of emission pro-
files, b-e zoomed in spectral regions with labeled emissions
region is far smaller than that of Root 1 (intensity of the roots and shoots. The soil moisture caused
0.03 versus 0.25 arbitrary units for Root 2 versus Root clumping on the slides; this became an issue as the
1, respectively). LIBS typically has limits of detection shockwave from the laser ablation process would
~10–100 ppm, so the qualitative verification of these move these clumps around or completely off the
micronutrients indicates their levels are above this in slide. This resulted in difficulties collecting repli-
the samples. cate spectra, as well as a significant level of noise
Soil from the greenhouse planters was tested in the spectra baseline. Emission peaks for many
as well. Unfortunately, the fresh soil had a mois- of the macronutrients that dominated the root and
ture level which interfered with the soils ability to shoot spectra were present, but lower mineral emis-
adhere to the double sided taped used for mounting sions were convoluted with the signal noise. Based
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Fig. 4 Stacked normalized and averaged LIBS spectra of the atmosphere species from the differences in how the samples
dried and cross sectioned root and shoot samples. The corre- ablate. Notice that in all spectra there is no emission on the
sponding normalized spectra from the fresh samples are over- shoulder of the H 656 nm peak that would correspond to the Li
laid in black for comparison. There are minimal changes to the seen in the soil sample
spectra; the greatest changes are the reduction in moisture and
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Fig. 5 Normalized and averaged LIBS spectra of the fresh and pelletized soil samples; a stacked plot to show similarity of emission
profiles, b-e zoomed in spectral regions with labeled emissions
at great concentrations in the soil indicated by their necessity to improve and understand the sustainabil-
increased relative intensities. The only mineral not ity of agriculture production. LIBS has been shown
detected in the plant samples was Li. to be a promising technique to demonstrate real-
time soil analysis at low cost and without the need
for intensive sample preparation. In this study, LIBS
Discussion was used to rapidly evaluate the elemental composi-
tion in small volume soil sample. The C, N, H, and
In-field detection of plant nutrients and toxic ele- O levels can clearly be measured with both elemen-
ments along with determining soil health assess- tal and molecular emissions and with no standard
ments via soil C and N measurements, are a interferents. Additionally, nutrient species Li, Na,
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Mg, K, Ca, Fe, Al, Si can all be clearly detected. In general, the fresh sample measurements com-
Although not seen in this sample, elements that are pare well with the prepared samples. This points
labeled trace, contaminant, and/or toxic elements towards the use of LIBS for in-situ analysis of plant
such as As, Cd, Hg and Pb can also be detected by tissues to rapidly analyze nutrient information. All
LIBS making it well suited for rapid screening of nutrient species identified in the fresh samples also
soil health and accumulation and cycling through appear in the prepared samples. There are minor dif-
plant uptake in agricultural and forest lands and ferences, such as concentrated Fe localities appearing
through the food web thereof (Duval et al. 2011; in the fresh sample scan and not in the prepared sam-
Liu et al. 2021). A full summary of the emissions ple scan, but this is due to the inhomogeneity of the
detected in this study are provided in Table 1. Fe in the samples rather than the preparation method.
Expanding the research tools available to char- However, this does draw attention to the importance
acterize and understand the nutrient element cor- of spatial scanning such that nutrients which form
relations among plant tissue types and soil depths clusters will be detected and not missed. It may also
is a critical need in the path to developing sustain- be of interest to researchers to examine how different
able perennial bioenergy crops that are co-optimized plant species distribute various micronutrients. It is
for biomass valorization aboveground and carbon also worth pointing out that the LIBS measurements
sequestration belowground. LIBS has been shown to on both the four-week old and 16-week old samples
require minimal material and minimal sample prepa- were completed without issue. This indicates that
ration to provide this information. This will be crucial future screening studies can start using samples start-
for rapidly identifying the performance of plant root ing at least at 4 weeks.
nutrient uptake from the soil and the subsequent dis- While the advantage of measuring fresh plant sam-
tribution of these nutrients throughout the plant. For ples is evident, there is some give and take associ-
example, in the samples studied it was evident that ated with measuring fresh soil versus pelletized soil.
Fe was abundant in the soil, present in local hot spots The fresh soil analysis does provide detection of all
in the roots, but absent in the tested plant shoot. The the same nutrients seen in the pelletized sample with
younger root also showed more concentrated Fe lev- little analysis time; however, the pelletized sample
els, but further sampling would be needed to associ- has a far lower level of baseline noise and permits
ate this trait with root maturity. Another mineral seen far more replicate measurements. For these reasons,
in the soil was Li, which was not seen in any plant both approaches are recommended. First, the fresh
samples. The ability to detect the Li levels in soils soil can be rapidly analyzed which may result in the
and plants may be useful for other studies (Shahzad detection of unexpected large levels of a given nutri-
et al. 2016; Kavanagh et al. 2018). These are but a ent. Secondly, the pelletized soil will confirm the pre-
few examples of the rapid analysis of the nutrient vious measurements and may also unveil lower-level
economy that can be accomplished using LIBS. nutrients which were hidden by the noise levels or
Table 1 List of major and Major Species Observed Major Species Observed Minor Species Observed
minor elemental species’ Wavelength Wavelength Wavelength
emission wavelengths (nm) (nm) (nm)
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Plant Soil (2024) 495:3–12 11
necessitate multiple shots to become better resolved Duval BD, Dijkstra P, Natali SM, Megonigal JP, Ketterer ME,
peaks. Along this chain of thought, the fresh soil Drake BG, Lerdau MT, Gordon G, Anbar AD, Hungate BA
(2011) Plant− soil distribution of potentially toxic elements
analysis may be improved by using a better tape to in response to elevated atmospheric CO2. Environ Sci Tech-
improve the soil adhesion to the slide or using a thin- nol 45(7):2570–2574. https://doi.org/10.1021/es102250u
ner layer of soil on the slide to mitigate plasma shock- Hahn DW (2009) Laser-induced breakdown spectroscopy for
wave dispersion of the soil sample. analysis of aerosol particles: the path toward quantitative
analysis. Spectroscopy (Santa Monica) 24(9)
Other improvements that could be made in the Hahn DW, Omenetto N (2012) Laser-induced breakdown
continued implementation of the LIBS for in situ spectroscopy (LIBS), part II: review of instrumental and
plant sample analysis would be to vary the spectrome- methodological approaches to material analysis and appli-
ter gating used. Elemental emissions from the excited cations to different fields. Appl Spectrosc 66(4):347–419
Harman-Ware AE, Sparks S, Addison B, Kalluri UC (2021)
plasma depend on the plasma temperature and elec- Importance of suberin biopolymer in plant function,
tron density. As LIBS plasmas are pulsed, they cool contributions to soil organic carbon and in the produc-
as the spectra are collected. By adjusting the temporal tion of bio-derived energy and materials. Biotechnol-
window observed for the measurement, different tran- ogy for Biofuels 14(1):1–21. https://doi.org/10.1186/
s13068-021-01892-3
sitions may be detected which may allow for better Jansson C, Wullschleger SD, Kalluri UC, Tuskan GA (2010)
distinguishment between species’ emission peaks. Phytosequestration: carbon biosequestration by plants
and the prospects of genetic engineering. Bioscience
Author contributions All authors contributed to the study 60(9):685–696. https://doi.org/10.1525/bio.2010.60.9.6
conception and design. Material preparation, data collection Kavanagh L, Keohane J, Cabellos GG, Lloyd A, Cleary J (2018)
and analysis were performed by Hunter B. Andrews, Ann M. Induced plant accumulation of lithium. Geosciences
Wymore, and Udaya C. Kalluri. The first draft of the manu- 8(2):56. https://doi.org/10.3390/geosciences8020056
script was written by Hunter B. Andrews and all authors com- Krajcarova L, Novotny K, Babula P, Provaznik I, Kucerova P,
mented on previous versions of the manuscript. All authors Adam V, Martin MZ, Kizek R, Kaiser J (2013) Copper
read and approved the final manuscript. transport and accumulation in spruce stems (Picea abies
(L.) Karsten) revealed by laser-induced breakdown spec-
Funding This work was supported by the United States troscopy. Int J Electrochem Sci 8:4485–4504
Department of Energy (DOE) Center for Bioenergy Innovation Kuppe CW, Schnepf A, von Lieres E, Watt M, Postma JA
(CBI) project. CBI is a Bioenergy Research Center supported (2022) Rhizosphere models: their concepts and appli-
by the Office of Biological and Environmental Research in the cation to plant-soil ecosystems. Plant Soil 474:17–55.
DOE Office of Science. This manuscript has been authored by https://doi.org/10.1007/s11104-021-05201-7
UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 Lal R (2004) Soil carbon sequestration impacts on
with the U.S. Department of Energy. global climate change and food security. Science
304(5677):1623–1627
Lal R (2018) Digging deeper: a holistic perspective of factors
Data availability The datasets generated are available from affecting soil organic carbon sequestration in agroecosys-
the corresponding author on reasonable request. tems. Glob Chang Biol 24(8):3285–3301. https://doi.org/
10.1111/gcb.14054
Declarations Liu W, Yang X, Duan L, Naidu R, Yan K, Liu Y, Wang X, Gao
Y, Chen Y (2021) Variability in plant trace element uptake
Competing interests The authors have no relevant financial across different crops, soil contamination levels and soil
or non-financial interests to disclose. properties in the Xinjiang Uygur autonomous region of
Northwest China. Sci Rep 11(1):1–13. https://doi.org/10.
1038/s41598-021-81764-w
Lynch JP (2019) Root phenotypes for improved nutrient cap-
ture: an underexploited opportunity for global agriculture.
New Phytol 223(2):548–564. https://doi.org/10.1111/nph.
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